Conserved immunomodulation and variation in host association by Xanthomonadales commensals in Arabidopsis root microbiota

Suppression of chronic Arabidopsis immune responses is a widespread but typically strain specific trait across the major bacterial lineages of the plant microbiota. We show by phylogenetic analysis of 1,765 Xanthomonadales genomes and in planta associations with representative strains that immunomodulation is a highly conserved, ancestral trait across this core order of the plant microbiota, and preceded specialization of these bacteria as host-adapted pathogens. Rhodanobacter R179, from the deepest branch of the Xanthomonadales, activates immune responses through EFR and SOBIR1 cell-surface receptor kinases, yet root transcriptomics suggest this commensal evades host immune perception upon prolonged association. R179 camouflage likely results from combined activities of the conserved ABC transporter permease (dssA) and the TonB-dependent transporter (dssB) and the selective elimination of immunogenic peptides derived from R179, other microbiota members, and the plant host. The ability of R179 to mask itself and other commensals from the plant immune system is consistent with a convergence of distinct root transcriptomes triggered by immunosuppressive or non-suppressive synthetic microbiota upon R179 co-inoculation. Although root load of R179 was not affected by simultaneous depletion of the host cell-surface receptor kinases EFR, FLS2 and SOBIR1 in mono-association, immunomodulation through dssAB provided R179 with a competitive advantage in a community lacking other immunosuppressive bacteria. Furthermore, root colonization of diverse commensal Xanthomonadales varied 1,000-fold despite conserved immunomodulation. We propose that extensive immunomodulation by Xanthomonadales is related to their adaptation to terrestrial habitats and might have contributed to variation in strain-specific root association, which together accounts for their prominent role in plant microbiota establishment.